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Are Floral Traits Adapted to Different Pollinators? Andrea B. Lemaitre

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Are Floral Traits Adapted to Different Pollinators? Andrea B. Lemaitre Generalized pollination system: Are floral traits adapted to different pollinators? Andrea B. Lemaitre, Carlos F. Pinto & Hermann M. Niemeyer Arthropod-Plant Interactions An international journal devoted to studies on interactions of insects, mites, and other arthropods with plants ISSN 1872-8855 Volume 8 Number 4 Arthropod-Plant Interactions (2014) 8:261-272 DOI 10.1007/s11829-014-9308-1 1 23 Your article is protected by copyright and all rights are held exclusively by Springer Science +Business Media Dordrecht. This e-offprint is for personal use only and shall not be self- archived in electronic repositories. If you wish to self-archive your article, please use the accepted manuscript version for posting on your own website. You may further deposit the accepted manuscript version in any repository, provided it is only made publicly available 12 months after official publication or later and provided acknowledgement is given to the original source of publication and a link is inserted to the published article on Springer's website. The link must be accompanied by the following text: "The final publication is available at link.springer.com”. 1 23 Author's personal copy Arthropod-Plant Interactions (2014) 8:261–272 DOI 10.1007/s11829-014-9308-1 ORIGINAL PAPER Generalized pollination system: Are floral traits adapted to different pollinators? Andrea B. Lemaitre • Carlos F. Pinto • Hermann M. Niemeyer Received: 29 January 2014 / Accepted: 20 May 2014 / Published online: 4 June 2014 Ó Springer Science+Business Media Dordrecht 2014 Abstract Flowers that are pollinated both during the day in bee-pollinated flowers. Flowers of E. chiloensis ssp. and at night could exhibit two different groups of chiloensis seem morphologically adapted to hawkmoth pollinators and produce two different sets of attractants and pollination, but diurnal and nocturnal pollinators contribute rewards. We explored the patterns of emission of flower to similar extents to reproductive success. Additionally, scents and production of nectar in the cactus Echinopsis diurnal and nocturnal pollinators showed a synergic effect chiloensis ssp. chiloensis, in relation to the patterns of on the product of fruit set and seed set. The results are activity of its diurnal and nocturnal pollinators. We mea- discussed in terms of the linkage between floral traits and sured frequency of flower visitors, analyzed floral scents, perception abilities and requirements of pollinators. measured nectar production and sugar concentration, and performed pollination exclusion experiments. Bees were Keywords Hawkmoth Á Bees Á Floral scents Á Nectar Á the main visitors at daytime and hawkmoths at nighttime. Pollination contribution Diurnal scents were dominated by several compounds that can attract a wide range of pollinators, whereas nocturnal scents were less diverse and were dominated by (E)-ner- Introduction olidol, a compound eliciting antennal responses in hawk- moths. Nectar volume and sugar concentration at night A pollination syndrome comprises the entire set of floral were similar to those recorded in hawkmoth-pollinated traits involved in the attraction of a particular pollinator flowers. Daytime nectar volume was higher than those (Proctor et al. 1996). Flowers with generalized pollination commonly found in bee-pollinated flowers, but similar to syndrome are those that attract more than one type of those found in flowers pollinated by several pollinators. pollinator (e.g., Young 2002; Schlumpberger and Badano Daytime sugar concentration was similar to those recorded 2005; Muchhala et al. 2008; Ortega-Baes et al. 2010; Schmid et al. 2010; Yokota and Yahara 2012) and are much more common than was thought until a few years ago Handling Editor: Lars Chittka. (Fleming et al. 2001). This syndrome may be an optimal strategy in highly variable environments, where the abun- Electronic supplementary material The online version of this article (doi:10.1007/s11829-014-9308-1) contains supplementary dance and distribution of pollinators fluctuate temporally material, which is available to authorized users. and spatially, because it prevents plant reproductive suc- cess to be negatively affected by the absence of particular & A. B. Lemaitre Á C. F. Pinto Á H. M. Niemeyer ( ) pollinators (Waser et al. 1996; Fleming et al. 2001). Departamento de Ciencias Ecolo´gicas, Facultad de Ciencias, Universidad de Chile, Casilla 653, Santiago, Chile Different types of pollinators may have different per- e-mail: niemeyer@abulafia.ciencias.uchile.cl ception abilities and requirements (e.g., Dell’Olivo and Kuhlemeier 2013; Schemske and Bradshaw 1999; Briscoe C. F. Pinto and Chittka 2001; Chittka and Raine 2006; Kim et al. Laboratorio de Ecologı´a Quı´mica, Facultad de Ciencias y Tecnologı´a, Universidad Mayor de San Simo´n. Parque La Torre, 2011). For example, hawkmoths are mainly attracted by Cochabamba, Bolivia olfactory cues (Yamamoto et al. 1969; Mechaber et al. 123 Author's personal copy 262 A. B. Lemaitre et al. 2002) and require large amounts of nectar with low sugar main visitors are bees. Because of the different perception concentration as reward (Opler 1983; Baker and Baker abilities and requirements of their floral pollinators, we 1983; Kaczorowski et al. 2005), and bees are mainly hypothesize that composition of flower scents, nectar vol- attracted by visual cues (Milet-Pinheiro et al. 2012) and umes, and sugar concentration in the nectar of E. chiloensis need lesser amounts of nectar with high sugar concentra- ssp. chiloensis differs between day and night, presenting tion (Opler 1983; Baker and Baker 1983). In this sense, characteristics related to the perception abilities and flowers that are pollinated both day and night may produce requirements of each group of pollinators. Furthermore, we flower scents (Dotterl et al. 2012) and nectar (Amorin et al. hypothesize that both groups of pollinators contribute to 2012) with different characteristics during the day and the reproductive success of the cactus. night, associated to their day and night pollinators, respectively. Moreover, for a generalized pollination syndrome to be Methods and materials considered as optimal, different groups of pollinators should contribute to the reproductive success of the plant Study area and study species (Fleming et al. 2001); these contributions depend in general on both the visitation rate and the effectiveness in pollen This study was conducted from November 2012 to Feb- transfer (e.g., Thomson 2000; Aigner 2004). Different ruary 2013 at the Reserva Nacional Rı´o Clarillo (RNRC), pollinators may differ in their frequency of visits and located 45 km southeast of Santiago (33°410–33°510S, pollination effectiveness (Waser et al. 1996). Hawkmoths 70°240–70°290W) between 860 y 3057 m.a.s.l. The climate are generally considered very effective pollinators: Due to corresponds to a mediterranean regime with rainy winters their large body size and their foraging behavior, they are and dry summers (Niemeyer et al. 2002). During the study capable of carrying large amounts of pollen along great period, the mean day temperature was 19 ± 0.5 °C and distances (Johnson 1995; Johnson and Liltved 1997), and a mean relative humidity was 54 ± 3 % (data from the agro- single visit can successfully fertilize a given flower meteorological station at RNRC; mean of data taken at (Willmot and Bu´rquez 1996). In contrast, bees are con- 09:00, 14:00, and 18:00, during the 4 months that the study sidered ineffective pollinators since, unlike hawkmoths lasted). The vegetation of the area is dominated by ever- which are nectar collectors, most bees are pollen collectors green plants of the sclerophyllous forest and matorral and the pollen mass transported, being mixed with nectar vegetational region (Gajardo 1993). E. chiloensis ssp. and resin, is not all available for pollination (Williams and chiloensis is endemic to central Chile from La Serena Adam 2010). (29°020S) to Talca (36°330S) (Luebert and Pliscoff 2006) Several species of cacti from temperate regions exhibit and exhibits different pollination syndromes along its dis- generalized pollination syndromes; their main nocturnal tribution. In its northern distribution (Coquimbo: 31°300S, visitors are moths while their main diurnal visitors are bees 71°060W), it exhibits a diurnal pollination syndrome where (de Viana et al. 2001; Schlumpberger and Badano 2005; flowers open between 06:00 and 07:00 h, remain open an Schlumpberger et al. 2009; Ortega-Baes et al. 2010; average of 8.5 h and their main visitors are bees (Ossa and Alonso-Pedano and Ortega-Baes 2012). Since the identity Medel 2011). In contrast, in the southern range (Rancagua: of the main pollinators changes drastically within a short 34°100S, 70°430W), it exhibits a generalized pollination period of time, these flowers are ideal models to test syndrome where flowers open between 18:00 and 20:00 h, hypotheses of character adaptation to different pollinators remain open for 20–22 h on average and their main diurnal (e.g., Dotterl et al. 2012; Amorin et al. 2012). visitors are bees, and their main nocturnal visitors are In this paper, we explore the patterns of emission of moths (Walter 2010). These previous studies have deter- flower scents and nectar production in Echinopsis chilo- mined the reproductive system of this cactus as self- ensis ssp. chiloensis, in relation to the patterns of activity of incompatible and totally dependent on cross-pollination. its diurnal and nocturnal pollinators. Flowers of the Individuals of E. chiloensis ssp. chiloensis were chosen columnar cactus E. chiloensis ssp. chiloensis (Colla) H. from among the population growing along the main river at Friedrich and G. D. Rowley exhibit traits that conform to a the RNRC, within an area of approximately 25 ha. Only hawkmoth pollination syndrome (Dobson 2006), i.e., they one flower per individual was used. Anthesis in the study are large, cone shaped, white colored, without nectar area began mostly between 18:00 and 21:00 h, the mean guides, open at dusk and stay open for periods that vary time of opening being ca.
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